ABSTRACT
Invasive species are among the most important, growing threats to food
security and agricultural systems. The Mediterranean fruit
fly Ceratitis capitata is one of the most damaging
representatives of a group of rapidly expanding species in the family
Tephritidae due to their wide host range and high invasiveness. Here, we
used restriction site-associated DNA sequencing (RADseq) to investigate
population genomic structure and phylogeographic history of medflies
collected from six sampling sites, including Africa (South Africa), the
Mediterranean (Spain, Greece), Latin America (Guatemala, Brazil) and
Australia. A total of 1,907 single nucleotide polymorphisms (SNPs)
showed two genetic clusters separating native and introduced ranges,
consistent with previous findings. In the introduced range, all
individuals were assigned to one genetic cluster except for those in
Brazil, which showed introgression of a genetic cluster that also
appeared exclusively in South Africa and could not be previously
identified using microsatellite markers. Moreover, the microbiome
variations in medfly populations from selected sampling sites was
assessed by amplicon sequencing of the 16S ribosomal RNA (V4 region). No
strong patterns of microbiome variation were detected across geographic
regions or host plants, except for the differentiation of the Brazilian
specimens which showed increased diversity and unique composition of its
microbiome compared to other sampling sites. The unique SNP patterns in
the Brazilian specimens could point to a direct migration route from
Africa with subsequent adaptation of the microbiota to the specific
conditions present in Brazil. These findings significantly improve our
understanding of the evolutionary history of global medfly invasions and
adaptation to newly colonised environments.
INTRODUCTION
Drastic environmental changes affecting natural and anthropogenic
ecosystems involve massive shifts in species’ geographical distributions
and cause worldwide invasions facilitated by the ability of certain
species to adapt to newly colonised environments (Heino, Virkkala, &
Toivonen, 2009). Invasive species have been associated with an estimated
1.3 trillion USD in economic losses and are responsible for diminishing
local species richness (Diagne et al., 2021). Therefore, frequent
interventions are required to control the damaging effects of invasive
species from new colonisation events. Large-scale range expansions and
intervention measures for pest control (e.g., pesticides, Sterile Insect
Technique (SIT)) have profound but poorly characterised effects on
population structure, invasion pathways, and adaptation to local
environments. Among agricultural insect pests, the family Tephritidae
(fruit flies) harbours several rapidly expanding species of great
concern, including the Mediterranean fruit fly Ceratitis
capitata (Wiedemann, 1824) (commonly known as medfly), a cosmopolitan,
polyphagous species with over 250 different hosts of fruit and
vegetables (White & Elson-Harris, 1992). In the past two
centuries, C. capitata has expanded from a presumed origin in
Sub-Saharan Africa to the Mediterranean basin and later spread to
tropical regions in all continents (Gasperi, Guglielmino, & Milani,
1991; Malacrida et al., 2007; Malacrida et al., 1992). Its range can
shift with climate change and commercial trade (Gutierrez & Ponti,
2011; Hill et al., 2016). It is considered one of the most successful
invaders worldwide and a significant economic pest to the fruit market,
estimated to cost more than 2 billion USD annually in losses (Sciarretta
et al., 2018).
Differences in local climate and exposure to various host plants and
natural enemies, reinforced by large geographic distances, may have
constrained gene flow, and resulted in differentiation of medfly
populations. Current knowledge of medfly population genetics supports
low levels of intercontinental connectivity between the native and
colonised ranges (Elfékih, Makni, & Haymer, 2010; Gasperi et al., 2002;
Karsten, Jansen van Vuuren, Addison, Terblanche, & Leung, 2015) but the
rate of dispersal among introduced populations remains unclear,
especially in Central and South America (Arias, Elfekih, & Vogler,
2018; Deschepper et al., 2021; Ruiz-Arce et al., 2020), despite its
importance for implementing pest control strategies. One of the
potential factors influencing the medfly’s propensity for dispersal and
adaptation to new environments is the interaction between the microbiome
and its host. It has been previously reported that specific microbiome
variants exist synergistically with insect hosts and might rapidly
spread across populations (Aharon et al., 2013). Evidence
from Drosophila melanogaster Meigen, 1830 suggests that shifts in
microbiome composition can alter population dynamics and, consequently,
might be considered a relevant driver of ecological and evolutionary
processes at the population level (Rudman et al., 2019). The medfly
receives its microbiota during oviposition via maternal inheritance
(Behar, Jurkevitch, & Yuval, 2008). The composition during larval
development is restructured, with microbial community shifts occurring
at different stages (Aharon et al., 2013; Malacrino, Campolo, Medina, &
Palmeri, 2018). Such knowledge dramatically enhances our understanding
of the influence of the microbial profile on insect development.
Exploring potential shifts of microbiota in introduced ranges could
reveal further information regarding the medfly’s colonisation
patterns.
The emergence of next-generation sequencing, including reduced
representation genome sequencing techniques such as Restriction
Associated DNA-tags sequencing (RADseq), has made it possible to study
the population diversity of non-model organisms at the genomic level
(Andrews et al., 2016, Davey & Blaxter, 2010). For example, RADseq has
been used to address biological questions on demography and dispersal of
invasive insect pests (Elfékih et al. 2018; McCormack, Hird, Zellmer,
Carstens, & Brumfield, 2013; Schmidt et al. 2020), patterns of gene
flow, phylogeography, and species delimitation (Eaton et al., 2013;
Elfékih et al. 2021; Emerson et al., 2010; Dong et al. 2021), microbial
association and local adaptation (Orantes et al. 2018; van Oppen et al.
2018).
Using RADseq data, we present the genetic relationships, gene flow
patterns, possible pathways of invasions, and cross-continent
colonisation routes of medfly populations collected from six regions
distributed worldwide. In addition, we examine genome-wide SNP variation
and explore the bacterial microbiome profile associated with each
sampling site and its possible correlation with the medfly presumed
dispersal routes.